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Phylogeny of the Acipenseriformes: Cytogenetic and Molecular Approaches

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Phylogeny of the Acipenseriformes: Cytogenetic and Molecular Approaches Environmental Biology of Fishes 48: 127–155, 1997. 1997 Kluwer Academic Publishers. Printed in the Netherlands. Phylogeny of the Acipenseriformes: cytogenetic and molecular approaches Vadim J. Birstein1, Robert Hanner2 & Rob DeSalle3 1 The Sturgeon Society, 331 West 57th Street, Suite 159, New York, NY 10019, U.S.A. 2 Department of Biology, University of Oregon, Eugene, OR 97405–1210, U.S.A. 3 Department of Entomology, American Museum of Natural History, New York, NY 10024, U.S.A. Received 20.3.1995 Accepted 21.3.1996 Key words: sturgeon, paddlefish, Huso, Acipenser, Scaphirhynchus, Pseudoscaphirhynchus, Polyodon, Pse- phurus, karyotype, chromosome, macrochromosome, microchromosome, genome, DNA content, 18S rRNA gene, cytochrome b, 12S mtrRNA gene, 16s mtrRNA gene, rate of molecular evolution, phylogeny, evolution Synopsis The review of the data on karyology and DNA content in Acipenseriformes shows that both extant families, the Polyodontidae and Acipenseridae, originated from a tetraploid ancestor which probably had a karyotype consisting of 120 macro- and microchromosomes and DNA content of about 3.2–3.8 pg per nucleus. The tetraploidization of the presumed 60-chromosome ancestor seems to have occurred at an early time of evolu- tion of the group. The divergence of the Acipenseridae into Scaphirhyninae and Acipenserinae occurred without polyploidization. Within the genus Acipenser, polyploidization was one of the main genetic mecha- nisms of speciation by which 8n and 16n-ploid species were formed. Individual gene trees constructed for sequenced partial fragments of the 18S rRNA (230 base pairs, bp), 12S rRNA (185 bp), 16S rRNA (316 bp), and cytochrome b (270 bp) genes of two Eurasian (A. baerii and A. ruthenus) and two American (A. transmonta- nus and A. medirostris) species of Acipenser, Huso dauricus, Pseudoscaphirhynchus kaufmanni, Scaphir- hynchus albus, and Polyodon spathula showed a low level of resolution; the analysis of a combined set of data for the four genes, however, gave better resolution. Our phylogeny based on molecular analysis had two major departures from existing morphological hypotheses: Huso dauricus is a sister-species to Acipenser instead of being basal to all acipenseriforms, and Scaphirhynchus and Pseudoscaphirhynchus do not form a monophy- letic group. The phylogenetic tree constructed for the cytochrome b gene fragments (with inclusion of 7 addi- tional species of Acipenser) supported the conclusion that octoploid species appeared at least three times within Acipenser. Introduction Amiidae, and Teleostei; Bemis et al. 1997 this vol- ume). Most ichthyologists regard Polypteridae as Although a few species of Acipenser require revi- the sister group of Acipenseriformes + Neopterygii sion, usually 24–25 extant sturgeon and two pad- (Patterson 1982). A comparison of partial sequenc- dlefish species, Polyodon spathula and Psephurus es of 28S rRNAs supported this relationship (Le et gladius, are included in the Acipenseriformes (Ro- al. 1993). In contrast to earlier works, Grande & Be- chard et al. 1991, Birstein 1993a). The extant mem- mis (1991) concluded that paddlefishes and stur- bers of this order form the monophyletic sister- geons are sister taxa, and that extinct Mesozoic gen- group of all extant Neopterygii (e.g., Lepisosteidae, era such as Chondrosteus lie outside this clade. Please indicate author’s corrections in blue, setting errors in red 110969 EBFI ART.NO 1621 (349) ORD.NO 231349.F 128 Within Acipenseriformes, all workers agree that ous occur in Central Asia (Nesov & Kaznyshkin the Acipenseridae and Polyodontidae diverged pri- 1983). or the Late Cretaceous (Berg 1948a, Yakovlev 1977, The China-western American group consists of 1986, Grande & Bemis 1991, Jin 1995, Grande & Be- Acipenser sinensis, A. dabryanus, A. medirostris, mis 1996, Bemis et al. 1997). Within the Acipenseri- and A. transmontanus; the external morphology of dae, the subfamily Scaphirhynchinae (Central the last two species is very similar (Findeis 1993). Asian species of Pseudoscaphirhynchus plus North All of these species seem to have common Tertiary American species of Scaphirhynchus) was tradi- roots (Artyukhin & Andronov 1990). The two ex- tionally considered the sister group of all other stur- tant paddlefish species also indicate a trans-Pacific geons (Berg 1905, Vasiliev 1985). Another interpre- pattern that is strengthened by the inclusion of fos- tation, based on osteology, was proposed by Findeis sil taxa, such as Eocene Crossopholis and Paleo- (1993, 1997 this volume), who found that Huso lacks cene Paleopsephurus (Grande & Bemis 1991, Jin many characters found in Acipenser, Scaphirhyn- 1995, Bemis et al. 1996, Grande & Bemis 1996). chus and Pseudoscaphirhynchus. On this basis, he The third group includes European and Amer- considered Scaphirhynchinae as a derived group ican Atlantic sturgeons (Vladykov & Greeley 1963, within Acipenseridae (Findeis 1997). This point of Kinzelbach 1987, Holcˇı´k et al. 1989). Probably, the view was disputed since the description of the Pseu- European A. sturio has many primitive characters doscaphirynchus species 120 years ago (Kessler of the genus (Nesov & Kaznyshkin 1977). Once con- 1877, Berg 1905), while other researchers consid- sidered a subspecies of A. sturio, the American At- ered Scaphirhyninae as the oldest group within Aci- lantic sturgeons were subsequently split off as a sep- penseridae (Bogdanov 1887). The examination of arate species, A. oxyrinchus (Vladykov & Greeley generic relationships within Acipenseriformes us- 1963). Then, two subspecies, A. o. oxyrinchus and ing molecular phylogenetic methods was one of the A. o. desotoi, were described within A. oxyrinchus main goals of this paper. (Vladykov 1955, Vladykov & Greeley 1963). The According to Nesov & Kaznyshkin (1977), extant origin and spread of the Atlantic sturgeon probably species of Acipenser belong to different evolution- reflect close Tertiary links between Europe and ary lineages which diverged long time ago. Artyuk- North America (Artyukhin & Andronov 1990). hin & Andronov (1990) and Artyukhin (1995) pro- The freshwater sturgeons of eastern North Amer- posed that there were at least four main regions in ica, belonging to the fourth group, the lake stur- which the speciation and spread of sturgeons took geon, A. fulvescens, and shortnose sturgeon, A. bre- place: (1) the Ponto-Caspian area; (2) China-west- virostrum, are possibly closely related (Vladykov & ern America; (3) the Atlantic area; and (4) eastern Greeley 1963) and may have originated on the East- North America. The group of Ponto-Caspian spe- ern coast of North America (Artyukhin & Andro- cies includes most of the Eurasian species (Acipen- nov 1990). ser gueldenstaedtii, A. persicus, A. stellatus, A. ruth- Evidence for monophyly of these four groups re- enus, A. nudiventris, Huso huso, A. baerii; Berg mains uncertain, and the relationships among them 1948b, Holcˇı´k et al. 1989, Pirogovsky et al. 1989, are unknown. Recently, Artyukhin (1995) publish- Shubina et al. 1989, Vlasenko et al. 1989a, b, Soko- ed a first phylogenetic tree based on general data of lov & Vasilev 1989a–c, Ruban 1997 this volume), as morphology, biogeography and karyology (but not well as Amur River endemics (A. schrenckii and the DNA content) of Acipenser. Atryukhin’s Huso dauricus; Artyukhin 1994, Krykhtin & Svir- scheme is the first modern attempt to reconstruct skii 1997 this volume), and, possibly, an Adriatic relationships within the genus Acipenser (see Be- species A. naccarii (Tortonese 1989, Rossi et al. mis et al. 1997, for a history of the 19th century at- 1991). The origin of Ponto-Caspian species might tempts to subdivide Acipenser into subgenera). have been associated with brackish-water deriva- Artyukhin & Andropov (1990) wrote: ‘It is quite tives of the Tethys Sea. The oldest extinct forms of evident that methods of biochemical genetics and the Ponto-Caspian group from the Upper Cretace- karyology, as well as paleontological data and cur- Please indicate author’s corrections in blue, setting errors in red 110969 EBFI ART.NO 1621 (349) ORD.NO 231349.F 129 Table 1. Chromosome numbers and DNA content in the Acipenseriformes, Lepisosteiformes, and Amiiformes1. Species Chromosome DNA content in Ploidy, n Reference numbers pg (according to the DNA content) Order Acipenseriformes family Polyodontidae North America Polyodon spathula Tennesse River, Alabama 120 – – Dingerkus & Howell (1976) Kentucky – 3.92 4 Tiersch et al. (1989) Missouri – 4.892 4 Blacklidge & Bidwell (1993) Moscow Aquarium, Russia – 3.172 4 Birstein et al. (1993) family Acipenseridae subfamily Acipenserinae Europe Acipenser gueldenstaedtii Volga River 250 ± 8 – – Birstein & Vasiliev (1987) 7.872 8 Birstein et al. (1993) Caspian Sea 247 ± 8 – – Vasiliev (1985) Sea of Azov 250 ± 8 – – Vasiliev (1985), Arefjev (1989a) Italy, cell culture 256 ± 8 – – Fontana et al. (1995) A. naccarii Italy 239 ± 7 – – Fontana & Colombo (1974) 246 ± 8 – – Fontana (1994) Italy, cell culture 246 ± 8 – – Fontana et al. (1995) A. nudiventris Black Sea 118 ± 2 – – Arefjev (1983), Vasiliev (1985) Aral Sea, Uzbekistan (Central Asia) – 3.902 4 Birstein et al. (1993) A. persicus Caspian Sea > 200 – – Fashkhami (pers. comm.) A. ruthenus Volga River 118 ± 2 – – Vasiliev (1985), Birstein & Vasiliev (1987) – 3.742 4 Birstein et al. (1993) Don River 118 ± 3 – – Arefjev (1989b) Danube, Yugoslavia 116 ± 4 – – Fontana et al. (1977) Danube, Slovakia 118 ± 3 – – Rab (1986) Italy (aquaculture) 118 ± 4 – – Fontana (1994)
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